www.nature.com/scientificreports OPEN Of city and village mice: behavioural adjustments of striped feld mice to urban environments Melanie Dammhahn1,2, Valeria Mazza1,2*, Annika Schirmer1, Claudia Göttsche1 & Jana A. Eccard1 A fundamental question of current ecological research concerns the drives and limits of species responses to human-induced rapid environmental change (HIREC). Behavioural responses to HIREC are a key component because behaviour links individual responses to population and community changes. Ongoing fast urbanization provides an ideal setting to test the functional role of behaviour for responses to HIREC. Consistent behavioural diferences between conspecifcs (animal personality) may be important determinants or constraints of animals’ adaptation to urban habitats. We tested whether urban and rural populations of small mammals difer in mean trait expression, fexibility and repeatability of behaviours associated to risk-taking and exploratory tendencies. Using a standardized behavioural test in the feld, we quantifed spatial exploration and boldness of striped feld mice (Apodemus agrarius, n = 96) from nine sub-populations, presenting diferent levels of urbanisation and anthropogenic disturbance. The level of urbanisation positively correlated with boldness, spatial exploration and behavioural fexibility, with urban dwellers being bolder, more explorative and more fexible in some traits than rural conspecifcs. Thus, individuals seem to distribute in a non-random way in response to human disturbance based on their behavioural characteristics. Animal personality might therefore play a key role in successful coping with the challenges of HIREC. Urbanisation is one of the fastest-occurring and most widespread human-induced environmental changes (e.g.1,2). As urban environments expand more and more across the globe, wildlife must either adjust to rapid changes and human-modifed landscapes, or experience severe declines and, ultimately, local extinction (e.g.2,3). Te urban environment presents wildlife with novel challenges, including an altered biotic environment with anthropogenic disturbances, modifed competitive interactions, new predators and parasites, as well as altered abiotic factors such as water, soil, light and air pollution, noise, soil sealing, fragmentation and trafc (e.g.2,4,5). As a result of these human-induced rapid environmental changes (HIREC5), ecosystems are experiencing sharp declines in biodiversity worldwide (e.g.1,2). A few species, however, are thriving and occur in high numbers in urban environments. A fundamental focus of current ecological and evolutionary research is to illuminate the drivers of the success of some animals in an urbanised world 3,6,7 because these “urban laboratories” might advance our understanding of fundamental eco-evolutionary processes and key theoretical concepts, including niche construction and community assembly as well as the role humans play in eco-evolutionary dynamics 8. Te ability of an animal to adjust to novel challenges is likely to contribute to its ultimate success in urban envi- ronments (e.g.3–5,9). Behavioural adaptations are expected to play a major role in coping with HIREC because behaviour largely determines how individuals interact with their surroundings (e.g.4,6,9,10) and behaviour links across fundamental levels of organisation from individual responses to population and community changes7. Also, behavioural responses typically occur faster, and are more rapidly reversible, than other responses to environmental change (e.g.5,7). In fact, behaviours of the so-called “urban adapters” ofen difer from those of their same-species rural counterparts (e.g.3,5,9,10). Two main factors are usually considered as potential drivers of diferences in behavioural responses to human disturbance in urban wildlife: behavioural fexibility and intrinsic behavioural characteristics (e.g.3,5,9). Behavioural fexibility (or reversible phenotypic plasticity) might allow some animals to habituate faster than others, become less sensitive to novel threats and fnd new alterna- tive solutions to the challenges of urban life (e.g.3,5,9). Several studies have demonstrated elevated behavioural fexibility within urban-adapter species (e.g.11–14). However, research also suggests that some diferences in the 1Department of Animal Ecology, Institute for Biochemistry and Biology, University of Potsdam, Potsdam, Germany. 2These authors contributed equally: Melanie Dammhahn and Valeria Mazza. *email: [email protected] SCIENTIFIC REPORTS | (2020) 10:13056 | https://doi.org/10.1038/s41598-020-69998-6 1 Vol.:(0123456789) www.nature.com/scientificreports/ behaviours of urban adapters cannot be explained by habituation/plasticity alone (e.g.15,16). Te second potential driver of behavioural adaptations to urban environments are intrinsic behavioural characteristics (e.g.3,5,9). Some individuals might just be better suited to reach and successfully colonize urban habitats than others (e.g.3,5,9). Between-individual behavioural diferences that are stable over time and across contexts are termed animal personality17, temperament18 or coping style 19. Individual animals can exhibit, for example, consistent levels of exploration, boldness, activity, sociability and aggression (e.g.17). Individuals with diferent behavioural types can play diferent ecological roles (e.g. exploiting diferent resources or ecological niches, being favoured at diferent stages of the dispersal/colonisation process) (e.g.20,21). “If some personality types are better suited to dealing with certain challenges than others, personality could determine how successfully individuals are able to occupy a range of diferent environments with diferent selective pressures”22. Following this line of reasoning, individual diferences in spatial exploration/dispersal tendencies, risk-taking and tolerance to human disturbance might promote the successful colonisation and settlement in urbanised habitats of only certain behavioural types (e.g.9). Among the axes of behavioural variation presenting potentially important implications for dispersal, settle- ment and establishment in novel environments, and particularly for coping with human-altered environments, are boldness and spatial exploration. Boldness is a personality trait that is characterized by individual difer- ences in willingness to take risks in a variety of contexts (e.g.23–25). Here, we defne risk-taking as the behaviour expressed in a risky situation and boldness as consistent individual diferences in risk-taking behaviour 17,26. Since behaviour under risk is a key determinant of both components of ftness (e.g.26,27), it is likely to be an ecologi- cally relevant personality trait. It is well established that boldness has ftness consequences (e.g.28), is heritable (e.g.29–31), and subject to selection (e.g.32,33). Furthermore, boldness is linked to life-history decisions such as dispersal (e.g.34,35), foraging (e.g.26,36,37), antipredator behaviour (e.g.24,36,38), and mating (e.g.39–41). Exploration refers to the gathering of information about the environment42, although the same term is also used to indicate the reaction to unfamiliar objects and places17. When applied to spatial exploration, a common problem faced by behavioural ecologists is to distinguish between the general locomotor activity and the gather- ing of environmental information (e.g.43–45). While the distinction is particularly sensitive for species that might use vision as a primary source of information, for taxa that rely predominantly on olfaction and touch to explore their environment/space, inter-individual variation in activity and spatial exploration are generally considered functionally integrated (e.g.43,46). Here, we defne exploration as the gathering of information about the environ- ment (e.g.42) and refer to spatial exploration as consistent individual diferences in exploratory behaviour in the context of space and in connection to movement (e.g.43,46), and use the term “general activity” for locomotion. Exploration presents a heritable component (e.g.47–51), afects survival (e.g.28) and reproductive success (e.g.52–54), indicating that inter-individual variation in exploration could create targets of selection43, and that it is likely to be an ecologically relevant personality trait. Furthermore, inter-individual variation in spatial exploration predicts dispersal tendency and space use in a diverse range of taxa (e.g.9,55–61), shares a genetic underpinning with dispersal, at least in some species (e.g.50), and is also suggested to facilitate the range expansion and invasive spread into new habitats (e.g.43,62). Investigating the diferences in boldness and spatial exploration between rural and urban populations might therefore help to illuminate the determinants of successful adaptation to urban colonisation, as well as reasons why most animals fail to adapt to rapidly changing environmental conditions. In the past few years, studies investigating behavioural adaptations to urban environments have fourished, focusing particularly on avian species (e.g.22,63–65). Here we focus on small, ground-dwelling species with more restricted dispersal abilities and aimed at test- ing whether urban and rural populations of a widely distributed rodent difer in behavioural fexibility and in intrinsic behavioural characteristics. Understanding the determinants of successful urbanisation of rodents is of particular interest because many species are urban dwellers or even synanthropic and